PARP-1 modulates deferoxamine-induced HIF-1α accumulation through the regulation of nitric oxide and oxidative stress

Journal of Cellular Biochemistry

Volumn 104, Issue 6, 2008, Pages 2248-2260

  Martínez Romero, Rubén ^a   Martínez Lara, Esther ^a   Aguilar Quesada, Rocío ^b   Peralta, Andreína ^b   Oliver, F Javier ^b   Siles, Eva ^a  

^a UNIVERSITY OF JAÉN   (Spain)

^b INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

Deferoxamine; HIF 1 ; Nitric oxide; Oxidative stress; PARP 1

Indexed keywords

DEFEROXAMINE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADRENOMEDULLIN; ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; DEFEROXAMINE; GENE EXPRESSION REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SUPEROXIDE DISMUTASE; THERMODYNAMICS; TIME FACTORS;

EID: 49049106519     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21781     Document Type: Article

References (67)

1. Agani FH, Pichiule P, Chavez JC, LaManna JC. 2000. The role of mitochondria in the regulation of hypoxia-inducible factor 1 expression during hypoxia. J Biol Chem 275:35863-35867.
2. Agani FH, Puchowicz M, Chavez JC, Pichiule P, LaManna J. 2002. Role of nitric oxide in the regulation of HIF-1alpha expression during hypoxia. Am J Physiol 283:C178-C186.
3. Beers KF Jr, Sizer IW. 1952. A spectrophotometric method of measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133-139.
4. Berchner-Pfannschmidt U, Yamac H, Trinidad B, Fandrey J. 2007. Nitric oxide modulates oxygen sensing by hypoxia-inducible factor 1-dependent induction of prolyl hydroxylase. J Biol Chem 282:1788-1796.
5. Bianchi L, Tacchini L, Cairo G. 1999. HIF-1-mediated activation of transferrin receptor gene transcription by iron chelation. Nucleic Acids Res 21:4223-4227.
6. Bowes J, Thiemermann C. 1998. Effects of inhibitors of the activity of poly (ADP-ribose) synthetase on the liver injury caused by ischaemia- reperfusion: a comparison with radical scavengers. Br J Pharmacol 124:1254-1260.
7. Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Braman RS, Hendrix SA. 1989. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal Chem 61:2715-2718.
9. Brune B, Zhou J. 2003. The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr Med Chem 10:845-855.
10. Cadenas E, Davies KJ. 2000. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222-230.
11. Callapina M, Zhou J, Schmid T, Kohl R, Brune B. 2005a. NO restores HIF-1alpha hydroxylation during hypoxia: role of reactive oxygen species. Free Radic Biol Med 39:925-936.
12. Callapina M, Zhou J, Schnitzer S, Metzen E, Lohr C, Deitmer JW, Brune B. 2005b. Nitric oxide reverses desferrioxamine- and hypoxia-evoked HIF-1alpha accumulation-implications for prolyl hydroxylase activity and iron. Exp Cell Res 306:274-284.
13. Carlberg I, Mannervik B. 1985. Glutathione reductase. Methods Enzymol 113:484-499.
14. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. 1998. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95:11715-11720.
15. 2 sensing. J Biol Chem 275:25130-25138.
16. Conde C, Mark M, Oliver FJ, Huber A, de Murcia G, Menissier-de Murcia J. 2001. Loss of poly(ADP-ribose) polymerase-1 causes increased tumour latency in p53-deficient mice. EMBO J 20:3535-3543.
17. Cuzzocrea S. 2005. Shock, inflammation and PAR. Pharmacol Res 52:72-82.
18. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. 1999. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342:249-268.
19. Digicaylioglu M, Lipton SA. 2001. Erythropoetin-mediated neuroprotection involves cross talk between Jak2 and NF-κB signalling cascades. Nature 412:641-647.
20. Ding Y, Zhou Y, Lai Q, Li J, Gordon V, Diaz FG. 2001. Long-term neuroprotective effect of inhibiting poly(ADP-ribose) polymerase in rats with middle cerebral artery occlusion using a behavioral assessment. Brain Res 915:210-217.
21. Dlaska M, Weiss G. 1999. Central role of transcription factor NF-IL6 for cytokine and iron-mediated regulation of murine inducible nitric oxide synthase expression. J Immunol 162:6171-6177.
22. Eliasson MJ, Sampei K, Mandir AS, Hum PD, Traystman RJ, Bao J, Pieper A, Wang ZQ, Dawson TM, Snyder SH, Dawson VL. 1997. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 3:1089-1095.
23. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54.
24. Fandrey J, Frede S, Jelkmann W. 1994. Role of hydrogen peroxide in hypoxia-induced erythropoietin production. Biochem J 303:507-510.
25. Flohé L, Günzler WA. 1984. Assays of glutathione peroxidase. Methods Enzymol 105:114-121.
26. Flohé L, Ötting F. 1984. Superoxide dismutase assays. Methods Enzymol 105:93-104.
27. Freret T, Valable S, Chazalviel L, Saulnier R, Mackenzie ET, Petit E, Bernaudin M, Boulouard M, Schumann-Bard P. 2006. Delayed administration of deferoxamine reduces brain damage and promotes functional recovery after transient focal cerebral ischemia in the rat. Eur J Neurosci 23:1757-1765.
28. Garayoa M, Martínez A, Lee S, Pío R, An WG, Neckers L, Trepel J, Montuenga LM, Ryan H, Johnson R, Gassmann M, Cuttitta F. 2000. Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol Endocrinol 14:848-862.
29. Gleadle JM, Ratcliffe PJ. 1998. Hypoxia and the regulation of physiologically relevant gene expression. Mol Med Today 4:122-129.
30. Grisham MB, Jourd'Heuil D, Wink DA. 1999. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites:implications in inflammation. Am J Physiol 276:G315-G321.
31. Groenendaal F, Shadid M, McGowan JE, Mishra OP, van Bel F. 2000. Effects of deferoxamine, a chelator of free iron, on NA(+), K(+)-ATPase activity of cortical brain cell membrane during early reperfusion after hypoxia-ischemia in newborn lambs. Pediatr Res 48:560-564.
32. Habig WH, Pabst MJ, Jakoby WB. 1974. Glutathione S-transferases. J Biol Chem 249:7130-7139.
33. Hagen T, Taylor CT, Lam F, Moncada S. 2003. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302:1975-1978.
34. Huang LE, Arany Z, Livingston DM, Bunn HF. 1996. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271:32253-32259.
35. Hurn PD, Koehler RC, Blizzard KK, Traystman RJ. 1995. Deferoxamine reduces early metabolic failure associated with severe cerebral ischemic acidosis in dogs. Stroke 26:688-695.
36. Kadikoylu G, Bolaman Z, Demir S, Balkaya M, Akalin N, Enli Y. 2004. The effects of desferrioxamine on cisplatin-induced lipid peroxidation and the activities of antioxidant enzymes in rat kidneys. Hum Exp Toxicol 23:29-34.
37. Kietzmann T, Fandrey J, Acker H. 2000. Oxygen radicals as messengers in oxygen-dependent gene expression. News Physiol Sci 15:202-208.
38. Kohl R, Zhou J, Brune B. 2006. Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Radic Biol Med 40:1430-1442.
39. López-Ramos JC, Martínez-Romero R, Molina F, Cañuelo A, Martí-nez-Lara E, Siles E, Peinado MA. 2005. Evidence of a decrease in nitric oxide-storage molecules following acute hypoxia and/or hypobaria, by means of chemiluminescence analysis. Nitric Oxide 13:62-67.
40. Martin-Oliva D, Aguilar-Quesada R, O'valle F, Munoz-Gamez JA, Martinez-Romero R, Garcia Del Moral R, Ruiz de Almodovar JM, Villuendas R, Piris MA, Oliver FJ. 2006. Inhibition of poly(ADP-ribose) polymerase modulates tumor-related gene expression, including hypoxia-inducible factor-1 activation, during skin carcinogenesis. Cancer Res 66:5744-5756.
41. Metzen E, Berchner-Pfannschmidt U, Stengel P, Marxsen JH, Stolze I, Klinger M, Huang WQ, Wotzlaw C, Hellwig-Burgel T, Jelkmann W, Acker H, Fandrey J. 2003a. Intracellular localisation of human HIF-1 alpha hydroxylases: Implications for oxygen sensing. J Cell Sci 116:1319-1326.
42. Metzen E, Zhou J, Jelkmann W, Fandrey J, Brune B. 2003b. Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol Biol Cell 14:3470-34781.
43. Mu D, Chang YS, Vexler ZS, Ferriero DM. 2005. Hypoxia-inducible factor 1alpha and erythropoietin upregulation with deferoxamine salvage after neonatal stroke. Exp Neurol 195:407-415.
44. Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsitohaina R, Muller S, de la Rubia G, Stoclet JC, de Murcia G. 1999. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J 18:4446-4454.
45. Palmer C, Roberts RL, Bero C. 1994. Deferoxamine posttreatment reduces ischemic brain injury in neonatal rats. Stroke 25:1039-1045.
46. Palmer LA, Semenza GL, Stoler MH, Johns RA. 1998. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-. Am J Physiol 274:L212-L219.
47. Quintero M, Brennan PA, Thomas GJ, Moncada S. 2006. Nitric oxide is a factor in the stabilization of hypoxia-inducible factor-1alpha in cancer: role of free radical formation. Cancer Res 66:770-774.
48. Ravati A, Ahlemeyer B, Becker A, Krieglstein J. 2000. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 866:23-32.
49. Saad SY, Najjar TA, Al Rikabi AC. 2001. The preventive role of deferoxamine against acute doxorubicin-induced cardiac, renal and hepatic toxicity in rats. Pharmacol Res 43:211-218.
50. Schreck R, Rieber P, Baeuerle PA. 1991. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10:2247-2258.
51. Semenza GL. 2005. New insights into nNOS regulation of vascular homeostasis. J Clin Invest 115:3128-3139.
52. Seo GS, Lee SH, Choi SC, Choi EY, Oh HM, Choi EJ, Park DS, Kim SW, Kim TH, Nah YH, Kim S, Kim SH, You SH, Jun CD. 2006. Iron chelator induces THP-1 cell differentiation potentially by modulating intracellular glutathione levels. Free Radic Biol Med 40:1502-1512.
53. Siles E, Martinez-Lara E, Núñez MI, Muñoz-Gámez JA, Martín-Oliva D, Valenzuela MT, Peinado MA, Ruiz de Almodóvar JM, Oliver FJ. 2005. PARP-1-dependent 3-nitrotyrosine protein modification after DNA damage. J Cell Biochem 96:709-715.
54. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, Mennini T, Heumann R, Cerami A, Ehrenreich H, Ghezzi P. 2000. Erythropoetin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 98:4044-4049.
55. Sogawa K, Numayama-Tsuruta K, Ema M, Abe M, Abe H, Fujii-Kuriyama Y. 1998. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci USA 95:7368-7373.
56. 2 tension. Proc Natl Acad Sci USA 92:5510-5514.
57. Wang M, Kirk JS, Venkataraman S, Domann FE, Zhang HJ, Schafer FQ, Flanagan SW, Weydert CJ, Spitz DR, Buettner GR, Oberley LW. 2005. Manganese superoxide dismutase suppresses hypoxic induction of hypoxia-inducible factor-1alpha and vascular endothelial growth factor. Oncogene 24:8154-8166.
58. Weiss G, Werner-Felmayer G, Werner ER, Grunewald K, Wachter H, Hentze MW. 1994. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J Exp Med 180:969-976.
59. Williams RE, Zweier JL, Flaherty JT. 1991. Treatment with deferoxamine during ischemia improves functional and metabolic recovery and reduces reperfusion-induced oxygen radical generation in rabbit hearts. Circulation 83:1006-1014.
60. Woo KJ, Lee TJ, Park JW, Kwon TK. 2006. Desferoxamine, an iron chelator, enhances HIF-1alpha accumulation via cyclooxygenase-2 signalling pathway. Biochem Biophys Res Commun 343:8-14.
61. Yang ZZ, Zhang AY, Yi FX, Li PL, Zou AP. 2003. Redox regulation of HIF-1alpha levels and HO-1 expression in renal medullary interstitial cells. Am J Physiol Renal Physiol 284:F1207-F1215.
62. Zaman K, Ryu H, Hall D, O'Donovan K, Lin KI, Miller MP, Marquis JC, Baraban JM, Semenza GL, Ratan RR. 1999. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21WAF1/cip1, and erythropoetin. J Neurosci 19:9821-9830.
63. Zhang Z, Ren J, Harlos K, McKinnon CH, Clifton IJ, Schofield CJ. 2002. Crystal structure of a clavaminate synthase-Fe(II)-2-oxoglutarate-substrate-NO complex: evidence for metal centered rearrangements. FEBS Lett 517:7-12.
64. Zhou HZ, Swanson RA, Simonis U, Ma X, Cecchini G, Gray MO. 2006. Poly(ADP-ribose) polymerase-1 hyperactivation and impairment of mitochondrial respiratory chain complex I function in reperfused mouse hearts. Am J Physiol Heart Circ Physiol 29:H714-H723.
65. Zhu H, Bunn HF. 1999. Oxygen sensing and signaling: impact on the regulation of physiologically relevant genes. Respir Physiol 115:239-247.
66. Zingarelli B, Cuzzocrea S, Zsengeller Z, Salzman AL, Szabo C. 1997. Protection against myocardial ischemia and reperfusion injury by 3-aminobenzamide, an inhibitor of poly (ADP-ribose) synthetase. Cardiovasc Res 36:205-215.
67. Zingarelli B, O'Connor M, Hake PW. 2003. Inhibitors of poly(ADP-ribose) polymerase modulate signal transduction pathways in colitis. Eur J Pharmacol 469:183-194.